Introduction

The genus Heterocapsa is composed of armored dinofla-gellates represented by relatively small planktonic species.Some Heterocapsa species such as Heterocapsa rotundata(Lohmann) Hansen and Heterocapsa triquetra (Ehrenberg)F. Stein have long been recognized to be cosmopolitan, redtide-forming taxa. In 1988, Heterocapsa circularisquamaHoriguchi was first found in Uranouchi Inlet, Kochi Prefec-ture, Japan, and has since spread along the coast of westernJapan accompanied by tremendous damage to bivalve aqua-culture (Horiguchi 1995, Matsuyama 1999). Since thisharmful species and its noxious effects, specifically on bi-valves, had never been reported it was described as the newspecies H. circularisquama (Horiguchi 1995). The previousdistribution of this novel harmful species remains unclear,however, its relatively higher optimum temperature forgrowth and a report of its occurrence from Hong Kongimply a recent transfer from tropical or subtropical waters

to Japan (Yamaguchi et al. 1997, Honjo et al. 1998, Iwatakiet al. 2002b, Iwataki & Matsuoka 2007). The continuedharmful impacts on aquaculture have promoted numerousinvestigations of the distribution and optimum conditionsfor growth of this species (e.g. Matsuyama et al. 1997, Ya-maguchi et al. 1997, Nagai et al. 2000, Yamaguchi et al.2001, Shiraishi et al. 2007). During previous studies of H.circularisquama, several undescribed species superficiallyresembling H. circularisquama had been observed; how-ever, it was difficult to define their taxonomic status at thattime.

The genus was originally described more than one hun-dred years ago (Stein 1883), and about 20 species have sofar been assigned to Heterocapsa. Since the presence of aresting cyst is unknown in Heterocapsa (Fensome et al.1993), species have been distinguished based on the mor-phology of the motile cell. Nonetheless, the generic criteriafor species assignment within Heterocapsa have continuedto change, resulting in some species descriptions unsuitablefor inclusion the genus, according to our present knowl-edge. Moreover, some of the morphological characters ofHeterocapsa that should be compared and contrasted, e.g.

Taxonomy and identification of the armored dinoflagellategenus Heterocapsa (Peridiniales, Dinophyceae)

MITSUNORI IWATAKI*

Institute for East China Sea Research, Nagasaki University, 1–14 Bunkyo, Nagasaki 852–8521, Japan

Received 13 September 2007; Accepted 28 January 2008

Abstract: The armored dinoflagellate genus Heterocapsa is composed of relatively small species, including a speciesresponsible for harmful red tides, H. circularisquama. Some Heterocapsa species such as H. rotundata and H. triquetrahave been well documented as red tide-forming species, but are not recognized as causing harmful effects. Followingsequential shellfish mass mortalities in the coastal waters of western Japan due to H. circularisquama red tides, thisspecies has attracted considerable interest. Many properties of this species, such as its distribution and growth charac-teristics, have been investigated to better understand the mechanisms involved in harmful red tide formation. Related tothe need for unambiguous identification of H. circularisquama, several unidentified (or undescribed) Heterocapsaspecies, which must be distinguished from the harmful taxon, have been detected sympatrically in regions where H. cir-cularisquama blooms occur. However, the taxonomic affiliation of these Heterocapsa species have not yet been deter-mined because several characteristics of Heterocapsa (e.g. body scale ultrastructure) have not yet been reported fromall described species due to the changing taxonomic criteria. After the taxonomic ambiguities in this genus were re-solved, cellular and body scale morphology of Heterocapsa were reinvestigated and several new species were described.In the present paper, the taxonomic history and morphological characters of the genus Heterocapsa are summarized.

Key words: body scale, dinoflagellate, Heterocapsa, morphology, nucleus, pyrenoid, red tide, taxonomy, thecalplates

Plankton Benthos Res 3(3): 135–142, 2008

* Corresponding author: Mitsunori Iwataki; E-mail, iwataki@nagasaki-u.ac.jp

Plankton & Benthos Research

© The Plankton Society of Japan

body scale ultrastructure, have not been reported in all thedescribed species. For taxonomic assignment of unidenti-fied species and unambiguous identification of H. circular-isquama, reliable criteria are required. Reinvestigations ofcommon morphological characters for the genus such astypical thecal plate arrangement (Po, cp, 5�, 3a, 7�, 6c, 5s,5�, 2��) and ultrastructure of the triradiate body scales cov-ering the cell surface have been carried out recently, and thetaxonomy of this genus was reassessed (Iwataki et al. 2003,2004). As a result of this work, fifteen species are now rec-ognized as possessing morphological characters common toHeterocapsa. In the present paper, the taxonomic historyand present status of the genus Heterocapsa are summa-rized and this reliability of morphological characters forspecies identification is discussed.

Taxonomic history of Heterocapsa

The genus Heterocapsa was originally established byStein in 1883 with the proposal of a new combination of thetype species H. triquetra from Glenodinium triquetrumEhrenberg (Stein 1883). Two species, H. umbilicata F. Steinand H. quadridentata F. Stein, were simultaneously de-scribed as new species (Stein 1883). In the systematics ofdinoflagellates at this time, two thecate genera, Peridiniumand Glenodinium, were distinguished based on whether thethecal plates (or sutures) were visible under a light micro-scope. As Stein (1883) could find the sutures only on theepitheca of G. triquetrum and the other two taxa, he tenta-tively established a new genus Heterocapsa, to include thespecies having a sutured epitheca and a flimsy hypotheca.The original etymology of the genus Heterocapsa, there-fore, denoted different types of the hemitheca. The cellshapes and thecal plate arrangements of the epitheca weresufficiently different to distinguish each of these threespecies from the other. These morphological and thecalplate variances represent the generic differences that arepresently accepted.

The next description of a Heterocapsa species was Hete-rocapsa pacifica Kofoid (Kofoid 1907). The cell shape ofthis species was somewhat similar to H. triquetra, but it dif-fered in several ways, including having a broader cellwidth, in the position of the nucleus and in possessing aprominent antapical spine. However, it contradicted theoriginal description of Heterocapsa, as the thecal plateswere not illustrated at all. Subsequently, Massart (1920) re-ported a new species Heterocapsa quinquecuspidata Mas-sart. The cell of H. quinquecuspidata resembled H. quadri-dentata in possessing five spines on the hypotheca. Onlythe thecal plates of the dorsal epitheca were illustrated.Four Heterocapsa species H. umbilicata, H. quadridentata,H. pacifica and H. quinquecuspidata have not been re-ported from any location since their original description,with only H. triquetra being reported by several authors(e.g. Schütt 1895, Lindemann 1924). The type species H.triquetra was re-examined and sutures were found also on

the hypotheca (Lindemann 1924), but this plate tabulationstill differed from later reports that have more recently beenaccepted (e.g. Morrill & Loeblich III 1981). During this pe-riod, cell shape was treated as the most fundamental or con-served character of Heterocapsa and the original criterionof the genus was neglected.

In the 1960s, all thecal plates were investigated in detailby light microscopy and their arrangements were adoptedas a criterion of the genus. Loeblich III (1968) describedthe new species Cachonina niei Loeblich III as the typespecies of a new genus Cachonina (Cachonina�Hetero-capsa) with the thecal plate arrangement illustrated as p.p.(apical pore plate�Po), 5�, 3a, 8�, 6c, 4s, 5�, 2��. Subse-quently, von Stosch (1969) reanalyzed the entire platearrangement of H. niei; Po, 6�, 3a, 8�, 6c, 4s (s.a. (anteriorsulcal plate), t (transitional plate), s.l. (left sulcal plate), s.p.(posterior sulcal plate)), 5�, 2��. A tiny canal plate was thendiscovered and mentioned as the sixth apical plate 6� (vonStosch 1969). This was the first report of a complete thecalplate tabulation to be worked out in detail for a member ofthe genus Heterocapsa (Loeblich III et al. 1981). Thereafterthe generic affiliation of each species was discussed basedon its thecal plate arrangement.

The next Cachonina species, C. illdefina Herman etSweeney, was described from a red tide sample collected inCalifornia (Herman & Sweeney 1976). This species namewas based on the English term “ill-defined” due to the frus-tration over its classification. The thecal plate tabulation ofC. illdefina was identical to C. niei; however, the configura-tion of the sulcal series and cell size were different. Trans-mission electron microscopy then revealed that C. illdefinahad tubular cytoplasmic invaginations within the pyrenoidmatrix, resembling those of H. triquetra as reported byDodge & Crawford (1971). In 1977, Balech analyzed in de-tail the thecal plates of C. illdefina, and considered it to besynonymous with C. niei based on the similarity of theirarrangements. In contrast to the opinion of Balech (1977),Morrill & Loeblich III reported a difference in cell sizerange between C. niei and C. illdefina (Morrill & LoeblichIII 1981). They also re-observed the complete thecal platearrangement of H. triquetra, 2pr, 5�, 3a, 7�, 6c, 7s, 5�, 1p,2��, and argued that the arrangements of Heterocapsa andCachonina were almost identical. Moreover they indicatedthe presence of organic body scales in these Cachoninaspecies, a character already observed in H. triquetra (Pen-nick & Clarke 1977). They then transferred C. niei and C.illdefina to Heterocapsa based on these common characterswith two new nomenclatural combinations, H. niei (Loe-blich III) Morrill et Loeblich III, and H. illdefina (Hermanet Sweeney) Morrill et Loeblich III (Morrill & Loeblich III1981). Since their proposal of these taxonomic combina-tions, the genus Cachonina has been considered to be a ju-nior synonym of Heterocapsa (Morrill & Loeblich III 1981,Fensome et al. 1993, Hansen 1995, Horiguchi 1995, 1997).During the same year, a new species Heterocapsa pygmaeaLoeblich III, Schmidt et Sherley was proposed (Loeblich III

136 M. IWATAKI

et al. 1981). The thecal plate arrangement of H. pygmaeawas given as; apical pore plate, canal plate, 5�, 3a, 7�, 5–7c(a.s., r.s., l.a.s., l.p.s., [? a.a.s. and p.a.s.] p.s.), 5�, 2��. Theyregarded the eighth precingular plate (8�) as the anteriorsulcal plate (as), which is a commonly accepted interpreta-tion at present. In the same paper, they also mentioned thatthe presence of body scales was a generic feature of Hete-rocapsa, and that scale sizes were a significant characteris-tic at the species level (Morrill & Loeblich III 1981).

Organic body scales, the distinctive feature of the genusHeterocapsa, were first reported from the type species H.triquetra (Pennick & Clarke 1977). Scales of H. triquetrawere observed in detail using TEM of both thin sectionsand whole mounts, and the three-dimensional structure wasillustrated. Thereafter, the presence of delicate organicbody scales on the cell surface was reported from Hetero-capsa species by several authors (Morrill & Loeblich III1981, 1983, Bullman & Roberts 1986). Subsequently, thedetailed structure of the scales of H. niei was examined andthis clearly illustrated the difference of this species from H.triquetra (Morrill & Loeblich III 1983). They mentionedthat the body scales were not only a common character ofthe genus Heterocapsa, but also that subtle differencesmight exist between the scales of each species.

During the 1970s, two species were assigned to Hetero-capsa, yet they have not been reported since. Heterocapsakollmeriana Swift et McLaughlin was reported from abloom in Phosphorescent Bay, Puerto Rico (Swift &McLaughlin 1970). The thecal plate arrangements and po-sition of the nucleus were unclear, and a detailed speciesdescription with a Latin diagnosis was not provided. Camp-bell (1973) transferred Peridinium chattonii Biecheler tothe genus Heterocapsa, proposing a new combination H.chattonii (Biecheler) Campbell. He also observed H. tri-quetra and considered its short first apical plate 1� as an im-portant taxonomic character of Heterocapsa. Anotherspecies of the genus, Heterocapsa minima Pomroy, was re-ported from the Celtic Sea, England (Pomroy 1989). Thisspecies was described mainly based on its small cell sizeand observations by scanning electron microscopy clearlyrevealed a thecal plate arrangement identical to Hetero-capsa, although body scales were not shown. H. minima isa rare species of Heterocapsa occurring in offshore waters.

In 1989, body scales similar to those in Heterocapsawere observed on the unarmored dinoflagellate Katodiniumrotundatum (Lohmann) Loeblich III, and their detailedstructure was reported (Hansen 1989). The scale structurewas not identical to previously reported scales in Hetero-capsa. Several years later, rather thin thecal plates with anarrangement similar to those of Heterocapsa were found onK. rotundatum, leading Hansen (1995) to propose a newcombination, H. rotundata. He also examined a culture ofHeterocapsa cf. minima and noted the differences in cellshape and body scale ultrastructure between H. rotundataand H. cf. minima. Thus the morphology of body scales hasbeen generally accepted to be the most important species

character. In the same year, the causative species of shell-fish mass mortalities, H. circularisquama, was described(Horiguchi 1995). Cell shape, size and thecal plate arrange-ment of H. circularisquama were rather similar to those ofH. illdefina, although the body scales clearly differed fromthe latter taxon. The species name of H. circularisquamameans circular scale and it was the first species establishedbased on body scale ultrastructure.

In the last decade, following the description of the harm-ful species H. circularisquama (Horiguchi 1995), sevenHeterocapsa species, H. arctica Horiguchi, H. horiguchiiIwataki, Takayama et Matsuoka, H. lanceolata Iwataki etFukuyo, H. orientalis Iwataki Botes et Fukuyo, H. ovataIwataki et Fukuyo, H. psammophila Tamura, Iwataki etHoriguchi, H. pseudotriquetra Iwataki, Hansen et Fukuyo,were described according to body scale morphologies(Horiguchi 1997, Iwataki et al. 2002a, 2003, 2004, Tamuraet al. 2005). Based on a comparison of morphological char-acteristics, common characters of the genus Heterocapsawere reexamined and the generic diagnosis was emendedby Iwataki & Fukuyo as: unicellular photosynthetic dinofla-gellate with thecal plates arranged as Po, cp, 5�, 3a, 7�, 6c,5s, 5�, 2�� and three-dimensional triradiate body scales(Iwataki et al. 2003). Iwataki et al. (2004) reanalyzed bodyscale fine structures of reported Heterocapsa species anddemonstrated the utility of scale structure for reliablespecies identification.

Armored dinoflagellates belonging to the genus Hetero-capsa are summarized in Fig. 5. Twenty species have so farbeen described or transferred to Heterocapsa. Of thesetaxa, five species without the characteristics of Hetero-capsa, H. umbilicata, H. quadridentata, H. quinquecuspi-data, H. kollmeriana, H. chattonii, are not treated as Hete-rocapsa at present. The other fifteen species (Figs. 3–5) arepresently recognized as valid Heterocapsa species.

Identification of Heterocapsa based on cellular morphol-ogy

Species of Heterocapsa are relatively small and sharecongruous morphological characters such as thecal platearrangement and reticulated chloroplasts located peripher-ally, making species difficult to identify using light mi-croscopy. Even though body scale fine structure (Figs. 1, 2)is required for the unambiguous identification of Hetero-capsa species (Iwataki et al. 2004), cellular characteristicssuch as cell size, shape, and the positions of the nucleusand pyrenoid are different in some species and they are alsouseful for tentative species identification. Cell shapes, withthe positions of the nucleus and pyrenoid, of recently recog-nized Heterocapsa are summarized in Figs. 3 and 4.

The average cell size of different Heterocapsa species isvariable, ranging from 7.4 mm for H. minima to 45 mm forH. pacifica (Kofoid 1907, Pomroy 1989). Size ranges ofmost species often overlap each other; therefore, it is diffi-cult to identify taxa based only on their cell sizes. On the

Taxonomy of Heterocapsa 137

138 M. IWATAKI

Fig. 1. Schematic illustrations of Heterocapsa niei, a motile cell with thecal plates including the apical pore plate (Po), canalplate (cp), apical plates (1�, 2�, 5�), precingular plates (1�, 7�), cingular plates (1c, 6c), sulcal plates (as, rs, las, lps, ps), post cin-gular plates (1�, 5�) and antapical plates (1�, 2��) (a), cell surface structure covered with body scales (b), and body scale structure(c). Thecal plates are located in amphiesmal vesicles underlying the cell membrane. Body scales are positioned on the cell mem-brane and covering the cell.

Fig. 2. Body scales of Heterocapsa species, whole mounts observed by TEM. H. arctica (a), H. circularisquama (b), H.horiguchii (c), H. illdefina (d), H. lanceolata (e), H. niei (f), H. orientalis (g), H. ovata (h), H. psammophila (i), H. pygmaea (j),H. rotundata (k), and H. triquetra (l). Body scale is composed of a reticulated triradiate basal plate and a three dimensional orna-ment composed of bars and spines; each species can be distinguished based on the scale structure, the shape of the basal plate,and the number of bars and spines. Scale bars�200 nm.

Taxonomy of Heterocapsa 139

Fig. 3. Photomicrographs of Heterocapsa species. H. circularisquama, light microscopy (a), fluorescence microscopy showingthecal plate arrangement (b), SEM (c), H. arctica (d), H. illdefina (e), H. horiguchii (f), H. lanceolata (g), H. niei (h), H. orien-talis (i), H. ovata (j), H. psammophila (k), H. pseudotriquetra (l), H. pygmaea (m), H. rotundata (n), and H. triquetra (o). N andPy indicate positions of the nucleus and pyrenoid, respectively. Scale bars�10 mm.

Fig. 4. Schematic drawings of species assigned to the genus Heterocapsa at present, showing cell shape and the positions of thenucleus (containing chromosomes: N) and pyrenoid (surrounded by starch sheaths: Py). Drawings of H. minima and H. pacificaare modified from Pomroy (1989) and Kofoid (1907), respectively; others are from Iwataki (2002) and Iwataki et al. (2002a,2003, 2004). Pyrenoid position of H. minima and thecal plate arrangement of H. pacifica are unknown.

other hand, cell shape seems to be stable in each species.Many Heterocapsa species exhibit an ellipsoidal or spheri-cal outline in the dorsal view and it is difficult to discern.However, several species possess specific features such asan apparently large epitheca compared to the hypotheca andan antapical horn. For example, the cell shape of H. trique-tra is rhomboid with an antapical horn, H. arctica is elon-gated with a large epitheca, H. lanceolata is lanceolate witha large epitheca and an antapical horn, and H. rotundata israther small with a large epitheca (Hansen 1995, Horiguchi1997, Iwataki et al. 2002a). Based on these specific charac-

ters, these four species can be identified under a light mi-croscope (Figs. 3–5). On the other hand, cells of H. orien-talis, H. ovata and H. pseudotriquetra are almost spherical(Iwataki et al. 2003, 2004). They can be discriminated fromother ellipsoidal species, but are difficult to distinguishfrom each other. Other ellipsoidal species including H. cir-cularisquama are also hard to identify under a light micro-scope.

Presence of a pyrenoid, surrounded by conspicuousstarch sheaths, which are visible under a light microscope,is one of the common characters of the genus (Fig. 3). Be-

140 M. IWATAKI

Fig. 5. A flow diagram for species identification of the genus Heterocapsa based on cell morphologies. Cell length is referableto Iwataki (2002).

cause the positions of the nucleus and pyrenoid are stableamong Heterocapsa species, their differences can be usefulfor differentiation of some species. Namely, for specieswith the nucleus located in the epitheca, the pyrenoid isusually positioned below the nucleus and vice versa (Figs.3, 4). Using this characteristic combined with its cell shape,several rather nondescript species such as ellipsoidal andspherical species can be distinguished from each other. Forexample, H. orientalis, H. ovata and H. pseudotriquetra arespherical and quite similar to each other, but only H. orien-talis has its nucleus in the hypotheca (Iwataki et al. 2003,2004). Among the ellipsoidal species, the nuclei of H. niei,H. psammophila and H. pygmaea are located in the hy-potheca, whereas that of H. horiguchii is positioned in theepitheca (Loeblich III et al. 1981, Morrill & Loeblich III1984, Iwataki et al. 2002a, Tamura et al. 2005). The nucleiof H. circularisquama and H. illdefina are elongatedthrough the cell (Herman & Sweeney 1976, Horiguchi1995); therefore, they are difficult to distinguish from eachother based on the nuclear position.

Consequently, about a half of all known Heterocapsaspecies can be distinguished based on the morphologicalcharacters such as cell shape and position of the organelles(Fig. 5). Since these characters can be observed under thelight microscope, they are quite useful for identification ofHeterocapsa species.

After harmful red tides of H. circularisquama appeared,morphological characters of Heterocapsa were reexaminedand the generic criteria were emended. Moreover, followinga detailed morphological evaluation, the presence of sixnew species, H. horiguchii, H. lanceolata, H. orientalis, H.ovata, H. psammophila and H. pseudotriquetra, was re-vealed recently only from Japanese coastal waters (Iwatakiet al. 2002a, 2003, 2004, Tamura et al. 2005). Since thecells of Heterocapsa are rather small and often hard toidentify, many undiscovered Heterocapsa species with un-known body scale structure are likely present in coastal wa-ters worldwide. Based on future comparisons, including thedescription of such species, a more comprehensive taxo-nomic system will be constructed for the genus Hetero-capsa.

Acknowledgements

The author thanks Dr Yasuwo Fukuyo of the Universityof Tokyo, Dr Kazumi Matsuoka of Nagasaki University, DrYoshiaki Hara of Yamagata University, Dr Takeo Horiguchiof Hokkaido University, Dr Gert Hansen of University ofCopenhagen, and Dr Haruyoshi Takayama, for their in-sightful criticisms and kind assistances. The author is grate-ful to Dr Gregory J. Doucette of NOAA/NOS, USA for acritical reading of the manuscript. Parts of the cultures usedfor the present study were provided from researchers at theFisheries Research Agency and Prefectural Fisheries Sta-tions.

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